Extended habit training reduces dopamine mediation of appetitive response expression

Abstract

A wide range of behaviors is impaired after disruption of dopamine (DA) transmission, yet behaviors that are reflexive, automatic, or elicited by salient cues often remain intact. Responses triggered by strong external cues appear to be DA independent. Here, we examined the possibility that a single behavior may become DA independent as a result of extended training. Rats were trained to execute a head-entry response to a cue signaling food delivery. Vulnerability of the response to D1 or D2 receptor blockade was assessed on day 3, 7, or 17 of 28-trial-per-day training. During the early stages of training, the D1 receptor antagonist R(+)-7-chloro-8-hydroxy-3-methyl-1-phenyl-2,3,4,5-tetrahydro-1H-3-benzazepine hydrochloride (SCH 23390) increased response latencies; however, the same behavior was unaffected by SCH 23390 in animals tested during the later stages of training. Other aspects of behavior such as locomotion and head-entry responses during the uncued intertrial interval remained vulnerable to SCH 23390 throughout the experiment. This D1-mediated response was unaffected by the D2 antagonist raclopride, even at a dose that strongly suppressed locomotion. The results provide strong evidence that a D1-dependent behavior becomes less dependent on DA with extended training. A number of fundamental neurobiological changes occur as behaviors become learned habits; at least for some responses, this change involves a shift from D1-mediated to D1-independent responding.

Figure 1.

Top, Mean ± SEM proportion of the 28 test trials that rats missed (i.e., showed a response latency of >10 s) as a function of the dose of the D₁ antagonist SCH 23390 (SCH) on test days 3, 7, and 17 (left) and for the 3-7 control group (right). The D₁ antagonist increased missed trials when administered during the third conditioning session (i.e., the day 3 group and the 3-7 control group). In contrast, rats that received the same doses of the D₁ antagonist on either day 7 or day 17 of training showed no increases in missed trials. This decrease in missed trials over the course of training mirrored and accounted for the reduced overall latency scores on days 7 and 17 (see Results). Bottom, The D₁ antagonist SCH 23390 produced locomotor suppression on all test days.

Figure 2.

Head entries into the food compartment (horizontal bars) were recorded during the period from 16 s before to 10 s after food delivery. Consecutive trials (1-28) are represented as successive rows on the y-axis (bottom to top). The vertical line at time 0 indicates the presentation of the auditory cue and food delivery 600 ms later. Additional time between trials (ITI time beyond this 26 s period) is not shown. On test day 3, SCH 23390 (SCH) disrupted head entries both during the ITI (before sec 0) and in response to the food cue (compare Saline with SCH on day 3; top left vs bottom left). By test day 17, the cue-elicited response had become invulnerable to D₁ antagonist challenge (bottom right), whereas execution of the same response during the ITI remained vulnerable to the D₁ antagonist (compare top right with bottom right). Although only representative rasters from days 3 and 17 are shown, performance on day 7 was similar to day 17 in that the cue-elicited response had become invulnerable to D₁ receptor blockade, whereas ITI responses remained D₁ dependent (see Results).